Impact of climate change on marine pelagic phenology and trophic mismatch

Phenology, the study of annually recurring life cycle events such as the timing of migrations and flowering, can provide particularly sensitive indicators of climate change. Changes in phenology may be important to ecosystem function because the level of response to climate change may vary across functional groups and multiple trophic levels. The decoupling of phenological relationships will have important ramifications for trophic interactions, altering food-web structures and leading to eventual ecosystem-level changes. Temperate marine environments may be particularly vulnerable to these changes because the recruitment success of higher trophic levels is highly dependent on synchronization with pulsed planktonic production. Using long-term data of 66 plankton taxa during the period from 1958 to 2002, we investigated whether climate warming signals are emergent across all trophic levels and functional groups within an ecological community. Here we show that not only is the marine pelagic community responding to climate changes, but also that the level of response differs throughout the community and the seasonal cycle, leading to a mismatch between trophic levels and functional groups.

Biodiversity and ecosystems: Change at the community level

Some commercial fish species of the northeast Atlantic Ocean have relocated in response to warming. The impact of warming on marine assemblages in the region may already be much greater than appreciated, however, with over 70% of common demersal fish species responding through changes in abundance, rather than range. The northeast Atlantic Ocean is one of the most productive marine ecoregions in the world with a substantial commercial fishery. It is also a region that has undergone particularly rapid warming over the past 50 years, up to four times faster than the global average1. Compared with other marine regions worldwide, the biological response in the northeast Atlantic Ocean has been particularly dramatic, reflecting this rapid warming. Studies have documented biogeographical movements in marine plankton of over 1,000 km northwards2 and advances in the onset of key life-history events by six to eight weeks3. In addition, there has been limited evidence of distributional shifts in some fish species along latitudinal and depth gradients in response to warming4, 5. Writing in Current Biology, Stephen Simpson and colleagues6 present the most comprehensive analysis so far of the impact of warming on commercially important European continental-shelf fish species in the region, and in doing so show that there has been a profound reorganization of local communities.

In hot water: zooplankton and climate change

An overview is provided of the observed and potential future responses of zooplankton communities to global warming. I begin by describing the importance of zooplankton in ocean ecosystems and the attributes that make them sensitive beacons of climate change. Global warming may have even greater repercussions for marine ecosystems than for terrestrial ecosystems, because temperature influences water column stability, nutrient enrichment, and the degree of new production, and thus the abundance, size composition, diversity, and trophic efficiency of zooplankton. Pertinent descriptions of physical changes in the ocean in response to climate change are given as a prelude to a detailed discussion of observed impacts of global warming on zooplankton. These manifest as changes in the distribution of individual species and assemblages, in the timing of important life-cycle events, and in abundance and community structure. The most illustrative case studies, where climate has had an obvious, tangible impact on zooplankton and substantial ecosystem consequences, are presented. Changes in the distribution and phenology of zooplankton are faster and greater than those observed for terrestrial groups. Relevant projected changes in ocean conditions are then presented, followed by an exploration of potential future changes in zooplankton communities from the perspective of different modelling approaches. Researchers have used a range of modelling approaches on individual species and functional groups forced by output from climate models under future greenhouse gas emission scenarios. I conclude by suggesting some potential future directions in climate change research for zooplankton, viz. the use of richer zooplankton functional groups in ecosystem models; greater research effort in tropical systems; investigating climate change in conjunction with other human impacts; and a global zooplankton observing system.

Effects on zooplankton of a warmer ocean: Recent evidence from the Northeast Pacific

The consequences for pelagic communities of warming trends in mid and high latitude ocean regions could be substantial, but their magnitude and trajectory are not yet known. Environmental changes predicted by climate models (and beginning to be confirmed by observations) include warming and freshening of the upper ocean and reduction in the extent and duration of ice cover. One way to evaluate response scenarios is by comparing how "similar" zooplankton communities have differed among years and/or locations with differing temperature. The subarctic Pacific is a strong candidate for such comparisons, because the same mix of zooplankton species dominates over a wide range of temperature climatologies, and observations have spanned substantial temperature variability at interannual-to-decadal time scales. In this paper, we review and extend copepod abundance and phenology time series from net tow and Continuous Plankton Recorder surveys in the subarctic Northeast Pacific. The two strongest responses we have observed are latitudinal shifts in centers of abundance of many species (poleward under warm conditions), and changes in the life cycle timing of Neocalanus plumchrus in both oceanic and coastal regions (earlier by several weeks in warm years and at warmer locations). These zooplankton data, plus indices of higher trophic level responses such as reproduction, growth and survival of pelagic fish and seabirds, are all moderately-to-strongly intercorrelated (vertical bar r vertical bar = 0.25-0.8) with indices of local and basin-scale temperature anomalies. A principal components analysis of the normalized anomaly time series from 1979 to 2004 shows that a single "warm-and-low-productivity" vs. "cool-and-high-productivity" component axis accounts for over half of the variance/covariance. Prior to 1990, the scores for this component were negative ("cool" and "productive") or near zero except positive in the El Nino years 1983 and 1987. The scores were strongly and increasingly positive ("warm" and "low productivity") from 1992 to 1998; negative from 1999 to 2002; and again increasingly positive from 2003-present. We suggest that, in strongly seasonal environments, anomalously high temperature may provide misleading environmental cues that contribute to timing mismatch between life history events and the more-nearly-fixed seasonality of insolation, stratification, and food supply. Crown Copyright (c) 2007 Published by Elsevier Ltd. All rights reserved.

Abundance of a chlorophyll a precursor and the oxidation product hydroxychlorophyll a during seasonal phytoplankton community progression in the Western English Channel

This study presents the first in-situ measurements of the chlorophyll a oxidation product, hydroxychlorophyll a as well as the chlorophyll a precursor, chlorophyll aP276 conducted over an annual cycle. Chlorophyll a oxidation products, such as hydroxychlorophyll a may be associated with the decline of algal populations and can act as an initial step in the degradation of chlorophyll a into products which can be found in the geochemical record, important for studying past climate change events. Here, hydroxychlorophyll a and chlorophyll aP276 were measured at the long-term monitoring station L4, Western Channel Observatory (UK, www.westernchannelobservatory.org) over an annual cycle (2012). Weekly measurements of phytoplankton species composition and abundance enabled detailed analysis of possible sources of hydroxychlorophyll a. Dinoflagellates, 2 diatom species, the prymnesiophyte Phaeocystis spp. and the coccolithophorid Emiliania huxleyi were all associated with hydroxychlorophyll a occurrence. However, during alternate peaks in abundance of the diatoms, no association with hydroxychlorophyll a occurred, indicating that the oxidation of chlorophyll a was dependant not only on species but also on additional factors such as the mode of mortality, growth limiting factor (i.e. nutrient concentration) or phenotypic plasticity. Surface sediment samples contained 10 times more hydroxychlorophyll a (relative to chlorophyll a) than pelagic particulate samples, indicating that more chlorophyll a oxidation occurred during sedimentation or at the sediment–water interface, than in the pelagic environment. In addition, chlorophyll aP276 correlated with chl-a concentration, thus supporting its assignment as a chl-a precursor.

Defining scenarios of future vectors of change in marine life and associated economic sectors

Addressing the multitude of challenges in marine policy requires an integrated approach that considers the multitude of drivers, pressures, and interests, from several disciplinary angles. Scenarios are needed to harmonise the analyses of different components of the marine system, and to deal with the uncertainty and complexity of the societal and biogeophysical dynamics in the system. This study considers a set of socio-economic scenarios to (1) explore possible futures in relation to marine invasive species, outbreak forming species, and gradual changes in species distribution and productivity; and (2) harmonise the projection modelling performed within associated studies. The exercise demonstrates that developing interdisciplinary scenarios as developed in this study is particularly complicated due to (1) the wide variety in endogeneity or exogeneity of variables in the different analyses involved; (2) the dual role of policy decisions as variables in a scenario or decisions to be evaluated and compared to other decisions; and (3) the substantial difference in time scale between societal and physical drivers.

Impact of climate change on Antarctic krill

Antarctic krill Euphausia superba (hereafter ‘krill’) occur in regions undergoing rapid environmental change, particularly loss of winter sea ice. During recent years, harvesting of krill has increased, possibly enhancing stress on krill and Antarctic ecosystems. Here we review the overall impact of climate change on krill and Antarctic ecosystems, discuss implications for an ecosystem-based fisheries management approach and identify critical knowledge gaps. Sea ice decline, ocean warming and other environmental stressors act in concert to modify the abundance, distribution and life cycle of krill. Although some of these changes can have positive effects on krill, their cumulative impact is most likely negative. Recruitment, driven largely by the winter survival of larval krill, is probably the population parameter most susceptible to climate change. Predicting changes to krill populations is urgent, because they will seriously impact Antarctic ecosystems. Such predictions, however, are complicated by an intense inter-annual variability in recruitment success and krill abundance. To improve the responsiveness of the ecosystem-based management approach adopted by the Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR), critical knowledge gaps need to be filled. In addition to a better understanding of the factors influencing recruitment, management will require a better understanding of the resilience and the genetic plasticity of krill life stages, and a quantitative understanding of under-ice and benthic habitat use. Current precautionary management measures of CCAMLR should be maintained until a better understanding of these processes has been achieved.

Aquatic Life Cycle Strategies: Survival in a variable environment. Occasional Publication of the Marine Biological Association 6

In a rapidly changing world it is essential that we should understand the factors controlling the sustainability of ecosystems. In aquatic ecosystems, both sensitivity and recoverability are influenced strongly by the life cycles of the organisms concerned. The response of individual species to change and their chances of survival in a variable environment can be affected dramatically by the timing and location of disturbances relative to their natural rhythms of fertilisation, dispersal and development. This book illustrates the wide range of issues that must be addressed to understand such relationships. Its purpose is to consider those aspects of life history that make aquatic organisms especially susceptible to (or adaptable to) changing environments -and hence to discuss links between impacts on individuals and the consequent effects on populations and communities.

Marine plankton phenology and life history in a changing climate: current research and future directions

Increasing availability and extent of biological ocean time series (from both in situ and satellite data) have helped reveal significant phenological variability of marine plankton. The extent to which the range of this variability is modified as a result of climate change is of obvious importance. Here we summarize recent research results on phenology of both phytoplankton and zooplankton. We suggest directions to better quantify and monitor future plankton phenology shifts, including (i) examining the main mode of expected future changes (ecological shifts in timing and spatial distribution to accommodate fixed environmental niches vs. evolutionary adaptation of timing controls to maintain fixed biogeography and seasonality), (ii) broader understanding of phenology at the species and community level (e.g. for zooplankton beyond Calanus and for phytoplankton beyond chlorophyll), (iii) improving and diversifying statistical metrics for indexing timing and trophic synchrony and (iv) improved consideration of spatio-temporal scales and the Lagrangian nature of plankton assemblages to separate time from space changes.

Temporal change in UK marine communities: trends or regime shifts?

A regime shift is a large, sudden, and long-lasting change in the dynamics of an ecosystem, affecting multiple trophic levels. There are a growing number of papers that report regime shifts in marine ecosystems. However, the evidence for regime shifts is equivocal, because the methods used to detect them are not yet well developed. We have collated over 300 biological time series from seven marine regions around the UK, covering the ecosystem from phytoplankton to marine mammals. Each time series consists of annual measures of abundance for a single group of organisms over several decades. We summarised the data for each region using the first principal component, weighting either each time series or each biological component (e.g. plankton, fish, benthos) equally. We then searched for regime shifts using Rodionov’s regime shift detection (RSD) method, which found regime shifts in the first principal component for all seven marine regions. However, there are consistent temporal trends in the data for six of the seven regions. Such trends violate the assumptions of RSD. Thus, the regime shifts detected by RSD in six of the seven regions are likely to be artefacts caused by temporal trends. We are therefore developing more appropriate time series models for both single populations and whole communities that will explicitly model temporal trends and should increase our ability to detect true regime shift events.

Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments

Recent changes in the seasonal timing (phenology) of familiar biological events have been one of the most conspicuous signs of climate change. However, the lack of a standardized approach to analysing change has hampered assessment of consistency in such changes among different taxa and trophic levels and across freshwater, terrestrial and marine environments. We present a standardized assessment of 25 532 rates of phenological change for 726 UK terrestrial, freshwater and marine taxa. The majority of spring and summer events have advanced, and more rapidly than previously documented. Such consistency is indicative of shared large scale drivers. Furthermore, average rates of change have accelerated in a way that is consistent with observed warming trends. Less coherent patterns in some groups of organisms point to the agency of more local scale processes and multiple drivers. For the first time we show a broad scale signal of differential phenological change among trophic levels; across environments advances in timing were slowest for secondary consumers, thus heightening the potential risk of temporal mismatch in key trophic interactions. If current patterns and rates of phenological change are indicative of future trends, future climate warming may exacerbate trophic mismatching, further disrupting the functioning, persistence and resilience of many ecosystems and having a major impact on ecosystem services.

Climate change and food safety: A review

Climate change and variability may have an impact on the occurrence of food safety hazards at various stages of the food chain, from primary production through to consumption. There are multiple pathways through which climate related factors may impact food safety including: changes in temperature and precipitation patterns, increased frequency and intensity of extreme weather events, ocean warming and acidification, and changes in contaminants’ transport pathways among others. Climate change may also affect socio-economic aspects related to food systems such as agriculture, animal production, global trade, demographics and human behaviour which all influence food safety. This paper reviews the potential impacts of predicted changes in climate on food contamination and food safety at various stages of the food chain and identifies adaptation strategies and research priorities to address food safety implications of climate change. The paper concludes that there is a need for intersectoral and international cooperation to better understand the changing food safety situation and in developing and implementing adaptation strategies to address emerging risks associated with climate change.